Inner envelope protein 32 is imported into chloroplasts by a novel pathway

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Date

2004

Journal Title

Journal ISSN

Volume Title

Type

Article

Publisher

The Company of Biologists Ltd

Series Info

Journal of cell science;117, 3975-3982

Abstract

The 32 kDa chloroplast inner envelope protein (IEP32) is imported into the organelle in the absence of a cleavable Nterminal pre-sequence. The ten N-terminal amino acids form an essential portion of this targeting information as deduced from deletion mutants. Recognition and translocation of IEP32 is not catalysed by the general chloroplast outer envelope translocon subunits Toc159, Toc75III and Toc34, because IEP32 import is neither inhibited by proteolytic removal of Toc34 and Toc159 nor by inhibition of the Toc75 import channel by CuCl2 or spermine. Import of IEP32 only requires ATP concentrations of below 20 µM indicating that stromal chaperones are not involved in the process, but that IEP32 might be directly inserted from the intermembrane space into the inner envelope by a so far unidentified pathway. IEP32 may require the assistance of Tic22, an intermembrane space translocon subunit for import as indicated by the presence of a chemical crosslinked product between both polypeptides.

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Keywords

Protein import, Targeting signal, Chloroplast, Envelope membranes

Citation

Bauer, J., Hiltbrunner, A. and Kessler, F. (2001). Molecular biology of chloroplast biogenesis: gene expression, protein import and intraorganellar sorting. Cell Mol. Life Sci. 58, 420-433. Bölter, B., Soll, J., Hill, K., Hemmler, R. and Wagner, R. (1999). A rectifying ATP-regulated solute channel in the chloroplastic outer envelope from pea. EMBO J. 18, 5505-5516. Caliebe, A., Grimm, R., Kaiser, G., Lübeck, J., Soll, J. and Heins, L. (1997). The chloroplastic protein import machinery contains a Rieske-type iron-sulfur cluster and a mononuclear iron-binding protein. EMBO J. 16, 7342-7350. Chen, X. and Schnell, D. J. (1999). Protein import into chloroplasts. Trends Cell Biol. 9, 222-227. Chou, M. L., Fitzpatrick, L. M., Tu, S. L., Budziszewski, G., Potter-Lewis, S., Akita, M., Levin, J. Z., Keegstra, K. and Li, H. M. (2003). Tic40, a membrane-anchored co-chaperone homolog in the chloroplast protein translocon. EMBO J. 22, 2970-2980. Cline, K., Werner-Washburne, M., Andrews, J. and Keegstra, K. (1984). Thermolysin is a suitable protease for probing the surface of intact pea chloroplasts. Plant Physiol. 75, 675-678. Eckart, K., Eichacker, L., Sohrt, K., Schleiff, E., Heins, L. and Soll, J. (2002). A Toc75-like protein import channel is abundant in chloroplasts. EMBO Rep. 3, 557-562. 3982 Ferro, M., Salvi, D., Brugière, S., Miras, S., Kowalski, S., Louwagie, M., Garin, J., Joyard, J. and Rolland, N. (2003). Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana. Mol. Cell. Proteomics 2, 325-345. Flügge, U. I. and Hinz, G. (1986). Energy dependence of protein translocation into chloroplasts. Eur. J. Biochem. 160, 563-570. Grimm, B., Ish-Shalom, D., Even, D., Glaczinski, H., Ottersbach, P., Ohad, I. and Kloppstech, K. (1989). The nuclear-coded chloroplast 22-kDa heatshock protein on Chlamydomonas. Evidence for translocation into the organ without translocation into the organelle without a processing step. Eur. J. Biochem. 182, 539-546. Heins, L., Mehrle, A., Hemmler, R., Wagner, R., Küchler, M., Hörmann, F., Sveshnikov, D. and Soll, J. (2002). The preprotein conducting channel at the inner envelope membrane of plastids. EMBO J. 21, 2616-2625. Hinnah, S. C., Hill, K., Wagner, R., Schlicher, T. and Soll, J. (1997). Reconstitution of a chloroplast protein import channel. EMBO J. 16, 7351- 7360. Hinnah, S. C., Wagner, R., Sveshnikova, N., Harrer, R. and Soll, J. (2002). The chloroplast protein import channel Toc75: pore properties and interaction with transit peptides. Biophys. J. 83, 899-911. Hirsch, S., Muckel, E., Heemeyer, F., von Heijine, G. and Soll, J. (1994). A receptor component of the chloroplast protein translocation machinery. Science 266, 1989-1992. Joyard, J., Billecocq, A., Barlett, S. G., Block, M. A. and Chua, N. H. (1983). Localization of polypeptides to the cytosolic side of the outer envelope membrane of spinach chloroplasts. J. Biol. Chem. 258, 10000- 10006. Keegstra, K. and Froehlich, J. E. (1999). Protein import into chloroplasts. Curr. Opin. Plant Biol. 2, 471-476. Kessler, F. and Blobel, G. (1996). Interaction of the protein import and folding machineries of the chloroplast. Proc. Natl. Acad. Sci. USA 93, 7684-7689. Kessler, F., Blobel, G., Patel, H. A. and Schnell, D. J. (1994). Identification of two GTP-binding proteins in the chloroplast protein import machinery. Science 266, 1035-1039. Kouranov, A. and Schnell, D. J. (1997). Analysis of the interactions of preproteins with the import machinery over the course of protein import into chloroplasts. J. Cell Biol. 139, 1677-1685. Kouranov, A., Chen, X., Fuks, B. and Schnell, D. J. (1998). Tic20 and Tic22 are new components of the protein import apparatus at the chloroplast inner envelope membrane. J. Chem. Biol. 143, 991-1002. Kouranov, A., Wang, H. and Schnell, D. J. (1999). Tic22 is targeted to the intermembrane space of chloroplasts ba a novel pathway. J. Biol. Chem. 274, 25181-25186. Küchler, M., Decker, S., Soll, J. and Heins, L. (2002). Protein import into chloroplasts involves redox-regulated proteins. EMBO J. 21, 6136-6145. Ma, Y., Kouranov, A., LaSala, S. and Schnell, D. J. (1996). Two components of the chloroplast protein import apparatus, IAP86 and IAP75, interact with the transit sequence during the recognition and translocation of precursor proteins at the outer envelope. J. Cell Biol. 134, 315-327. Miras, S., Salvi, D., Ferro, M., Grunwald, D., Garin, J., Joyard, J. and Rolland, N. (2002). Non-canonical transit peptide for import into the chloroplast. J. Biol. Chem. 277, 47770-47778. Nielsen, E., Akita, M., Davila-Aponte, J. and Keegstra, K. (1997). Stable association of chloroplastic precursors with protein translocation complexes that contain proteins from both envelope membranes and a stromal Hsp100 molecular chaperone. EMBO J. 16, 935-946. Oblong, J. E. and Lamppa, G. K. (1992). Identification of two structurally related proteins involved in proteolytic processing of precursors targeted to the chloroplast. EMBO J. 11, 4401-4409. Olsen, L. J., Theg, S. M., Selman, B. R. and Keegstra, K. (1989). ATP is required for the binding of precursor proteins to chloroplasts. J. Biol. Chem. 264, 6724-6729. Pfanner, N. and Geissler, A. (2001). Versatility of the mitochondrial protein import machinery. Nat. Rev. Mol. Cell. Biol. 2, 339-349. Pohlmeyer, K., Soll, J., Steinkamp, T., Hinnah, S. C. and Wagner, R. (1998). Isolation and characterization of an amino-selective channel protein present in the chloroplastic outer envelope membrane. Proc. Natl. Acad. Sci. USA 94, 9504-9509. Schindler, C., Hracky, R. and Soll, J. (1987). Protein transport in chloroplasts: ATP is prerequisit. Z. Naturforsch. Sect. C 42, 103-108. Schleiff, E. and Klösgen, R. B. (2001). Without a little help from ‘my’ friends: direct insertion of proteins into chloroplast membranes? Biochim. Biophys. Acta 1541, 22-23. Schleiff, E., Jelic, M. and Soll, J. (2003). A GTP-driven motor moves proteins across the outer envelope of chloroplasts. Proc. Natl. Acad. Sci. USA 100, 4604-4609. Schnell, D. J., Kessler, F. and Blobel, G. (1994). Isolation of components of the chloroplast protein import machinery. Science 266, 1007-1012. Seedorf, M. and Soll, J. (1995). Copper chloride, an inhibitor of protein import into chloroplasts. FEBS Lett. 367, 19-22. Seedorf, M., Waegemann, K. and Soll, J. (1995). A constituent of the chloroplast import complex represents a new type of GTP-binding protein. Plant J. 7, 401-411. Soll, J. (2002). Protein import into chloroplasts. Curr. Opin. Plant Biol. 5, 529- 535. Stahl, T., Glockmann, C., Soll, J. and Heins, L. (1999). Tic40, a new “old” subunit of the chloroplast protein import translocon. J. Biol. Chem. 274, 37467-37472. Theg, S. M., Bauerle, C., Olsen, L. J., Selman, B. R. and Keegstra, K. (1989). Internal ATP is the only energy requirement for the translocation of precursor proteins across chloroplastic membranes. J. Biol. Chem. 264, 6730-6736. Tranel, P. J. and Keegstra, K. (1996). A novel bipartite transit peptide target OEP75 to the outer membrane of chloroplastic envelope. Plant Cell 8, 2093- 2104. Tranel, P. J., Fröhlich, J., Goyal, A. and Keegstra, K. A. (1995). Component of the chloroplastic protein import apparatus is targeted to the outer envelope membrane via a novel pathway. EMBO J. 14, 2436-2446. von Heijne, G. and Nishikawa, K. (1991). Chloroplast transit peptides. The perfect random coil? FEBS Lett. 278, 1-3. Waegemann, K. and Soll, J. (1991). Characterization of the protein import apparatus in isolated outer envelopes of chloroplasts. Plant J. 1, 149-159. Waegemann, K. and Soll, J. (1995). Characterization and isolation of the chloroplast protein import machinery. Meth. Cell Biol. 50, 255-267.